Truncating NFKB1 variants cause combined NLRP3 inflammasome activation and type I interferon signaling and predispose to necrotizing fasciitis

Cell Rep Med. 2024 Apr 16;5(4):101503. doi: 10.1016/j.xcrm.2024.101503. Epub 2024 Apr 8.

Abstract

In monogenic autoinflammatory diseases, mutations in genes regulating innate immune responses often lead to uncontrolled activation of inflammasome pathways or the type I interferon (IFN-I) response. We describe a mechanism of autoinflammation potentially predisposing patients to life-threatening necrotizing soft tissue inflammation. Six unrelated families are identified in which affected members present with necrotizing fasciitis or severe soft tissue inflammations. Exome sequencing reveals truncating monoallelic loss-of-function variants of nuclear factor κ light-chain enhancer of activated B cells (NFKB1) in affected patients. In patients' macrophages and in NFKB1-variant-bearing THP-1 cells, activation increases both interleukin (IL)-1β secretion and IFN-I signaling. Truncation of NF-κB1 impairs autophagy, accompanied by the accumulation of reactive oxygen species and reduced degradation of inflammasome receptor nucleotide-binding oligomerization domain, leucine-rich repeat-containing protein 3 (NLRP3), and Toll/IL-1 receptor domain-containing adaptor protein inducing IFN-β (TRIF), thus leading to combined excessive inflammasome and IFN-I activity. Many of the patients respond to anti-inflammatory treatment, and targeting IL-1β and/or IFN-I signaling could represent a therapeutic approach for these patients.

Keywords: NFKB1; NLRP3 inflammasome; Type I interferon response; autoinflammation; autoinflammatory disease; autophagy; macrophages; monocytes; necrotizing fasciitis; severe soft-tissue inflammation; truncating mutation of NFKB1.

MeSH terms

  • Fasciitis, Necrotizing*
  • Humans
  • Immunity, Innate
  • Inflammasomes / metabolism
  • Inflammation / metabolism
  • Interferon Type I*
  • NF-kappa B p50 Subunit
  • NLR Family, Pyrin Domain-Containing 3 Protein / genetics
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism

Substances

  • Inflammasomes
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Interferon Type I
  • NFKB1 protein, human
  • NF-kappa B p50 Subunit